Correlations of noninvasive BOLD and TOLD MRI with pO2 and relevance to tumor radiation response

Magnetic Resonance in Medicine

Volumn 71, Issue 5, 2014, Pages 1863-1873

  Hallac, Rami R ^a   Zhou, Heling ^a   Pidikiti, Rajesh ^b   Song, Kwang ^b   Stojadinovic, Strahinja ^b   Zhao, Dawen ^a   Solberg, Timothy ^b   Peschke, Peter ^c   Mason, Ralph P ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

BOLD; carbogen; hypoxia; MRI; oximetry; oxygen; radiation response

Indexed keywords

IRRADIATION; MAGNETIC RESONANCE IMAGING; OXYGEN; OXYGENATION;

BOLD; CARBOGEN; HYPOXIA; OXIMETRY; RADIATION RESPONSE;

TUMORS;

CARBOGEN; HEXAFLUOROBENZENE; OXYGEN; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD OXYGENATION LEVEL DEPENDENT MAGNETIC RESONANCE IMAGING; BOLD SIGNAL; CANCER RADIOTHERAPY; CONTRAST ENHANCEMENT; CONTROLLED STUDY; INTERMETHOD COMPARISON; IRRADIATION; MALE; NON INVASIVE PROCEDURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OXYGEN TENSION; PROSTATE CANCER; RADIATION DOSE DISTRIBUTION; RADIATION RESPONSE; RAT; TISSUE OXYGENATION LEVEL DEPENDENT MAGNETIC RESONANCE IMAGING; TUMOR GROWTH; ANIMAL; COMPARATIVE STUDY; METABOLISM; MOLECULAR IMAGING; OXIMETRY; PATHOLOGY; PROCEDURES; PROSTATIC NEOPLASMS; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; STATISTICS; TREATMENT OUTCOME;

ANIMALS; MAGNETIC RESONANCE IMAGING; MALE; MOLECULAR IMAGING; OXIMETRY; OXYGEN; PROSTATIC NEOPLASMS; RATS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; STATISTICS AS TOPIC; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL;

EID: 84899458497     PISSN: 07403194     EISSN: 15222594     Source Type: Journal    
DOI: 10.1002/mrm.24846     Document Type: Article

References (60)

1. Tatum JL, Kelloff GJ, Gillies RJ, et al. Hypoxia: importance in tumor biology, noninvasive measurement by imaging, and value of its measurement in the management of cancer therapy. Int J Radiat Biol 2006; 82: 699-757.
2. Gray L, Conger A, Ebert M, Hornsey S, Scott O,. The concentration of oxygen dissolved in tissues at time of irradiation as a factor in radiotherapy. Br J Radiol 1953; 26: 638-648.
3. Höckel M, Schlenger K, Aral B, Mitze M, Schäffer U, Vaupel P,. Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res 1996; 56: 4509-4515.
4. Fyles AW, Milosevic M, Wong R, et al. Oxygenation predicts radiation response and survival in patients with cervix cancer. Radiother Oncol 1998; 48: 149-156.
5. Brizel DM, Sibly GS, Prosmitz LR, Scher RL, Dewhirst MW,. Tumor hypoxia adversely affects the prognosis of carcinoma of the head and neck. Int J Radiat Oncol Biol Phys 1997; 38: 285-289.
6. 2 ratio predicts for outcome in patients with localized prostate cancer: long-term results. Int J Radiat Oncol Biol Phys 2012; 82: E433-E439.
7. Alonzi R, Padhani AR, Maxwell RJ, et al. Carbogen breathing increases prostate cancer oxygenation: a translational MRI study in murine xenografts and humans. Br J Cancer 2009; 100: 644-648.
8. 2) with oxygen electrode measurements: a pilot study in men with prostate cancer. Int J Radiat Biol 2009; 85: 805-813.
9. Rijpkema M, Kaanders JH, Joosten FB, van der Kogel AJ, Heerschap A,. Effects of breathing a hyperoxic hypercapnic gas mixture on blood oxygenation and vascularity of head-and-neck tumors as measured by magnetic resonance imaging. Int J Radiat Oncol Biol Phys 2002; 53: 1185-1191.
10. Muller A, Remmele S, Wenningmann I, et al. Intracranial tumor response to respiratory challenges at 3.0 T: impact of different methods to quantify changes in the MR relaxation rate R 2. J Magn Reson Imaging 2010; 32: 17-23.
11. Taylor NJ, Baddeley H, Goodchild KA, et al. BOLD MRI of human tumor oxygenation during carbogen breathing. J Magn Reson Imaging 2001; 14: 156-163.
12. O'Connor JPB, Naish JH, Parker GJM, et al. Preliminary study of oxygen-enhanced longitudinal relaxation in MRI: a potential novel biomarker of oxygenation changes in solid tumors. Int J Radiat Oncol Biol Phys 2009; 75: 1209-1215.
13. Hallac RR, Ding Y, Yuan Q, McColl RW, Lea J, Sims RD, Weatherall PT, Mason RP,. Oxygenation in cervical cancer and normal uterine cervix assessed using blood oxygenation level-dependent (BOLD) MRI at 3T. NMR Biomed 2012; 25: 1321-1330.
14. Jiang L, Weatherall PT, McColl RW, Tripathy D, Mason RP,. Blood oxygenation level-dependent (BOLD) contrast magnetic resonance imaging (MRI) for prediction of breast cancer chemotherapy response: a pilot study. J Magn Reson Imaging 2013; 37: 1083-1092.
15. Neeman M, Dafni H, Bukhari O, Braun RD, Dewhirst MW,. In vivo BOLD contrast MRI mapping of subcutaneous vascular function and maturation: validation by intravital microscopy. Magn Reson Med 2001; 45: 887-898.
16. McPhail LD, Robinson SP,. intrinsic susceptibility mr imaging of chemically induced rat mammary tumors: relationship to histologic assessment of hypoxia and fibrosis. Radiology 2010; 254: 110-118.
17. Rodrigues LM, Howe FA, Griffiths JR, Robinson SP,. Tumor R-2 * is a prognostic indicator of acute radiotherapeutic response in rodent tumors. J Magn Reson Imaging 2004; 19: 482-488.
18. 19F MRI to investigate tumor oxygenation. Magn Reson Med 2009; 62: 357-364.
19. Elas M, Williams BB, Parasca A, et al. Quantitative tumor oxymetric images from 4D electron paramagnetic resonance imaging (EPRI): methodology and comparison with blood oxygen level-dependent (BOLD) MRI. Magn Reson Med 2003; 49: 682-691.
20. 2) inside tumors? Magn Reson Med 2002; 48: 980-986.
21. Jordan BF, Crokart N, Baudelet C, Cron GO, Ansiaux R, Gallez B,. Complex relationship between changes in oxygenation status and changes in R-2: the case of insulin and NS-398, two inhibitors of oxygen consumption. Magn Reson Med 2006; 56: 637-643.
22. Baudelet C, Gallez B,. Current issues in the utility of blood oxygen level dependent MRI for the assessment of modulations in tumor oxygenation. Curr Med Imaging Rev 2005; 1: 229-43.
23. Howe FA, Robinson SP, McIntyre DJO, Stubbs M, Griffiths JR,. Issues in flow and oxygenation dependent contrast (FLOOD) imaging of tumours. NMR Biomed 2001; 14: 497-506.
24. Fan XB, River JN, Zamora M, Al-Hallaq HA, Karczmar GS,. Effect of carbogen on tumor oxygenation: combined fluorine-19 and proton MRI measurements. Int J Radiat Oncol Biol Phys 2002; 54: 1202-1209.
25. Dunn JF, O'Hara JA, Zaim-Wadghiri Y, et al. Changes in oxygenation of intracranial tumors with carbogen: a BOLD MRI and EPR oximetry study. J Magn Reson Imaging 2002; 16: 511-521.
26. Al-Hallaq HA, River JN, Zamora M, Oikawa H, Karczmar GS,. Correlation of magnetic resonance and oxygen microelectrode measurements of carbogen-induced changes in tumor oxygenation. Int J Radiat Oncol Biol Phys 1998; 41: 151-159.
27. Robinson SP, Howe FA, Rodrigues LM, Stubbs M, Griffiths JR,. Magnetic resonance imaging techniques for monitoring changes in tumor oxygenation and blood flow. Semin Radiat Oncol 1998; 8: 198-207.
28. Young IR, Clarke GJ, Bailes DR, Pennock JM, Doyle FH, Bydder GM,. Enhancement of relaxation rate with paramagnetic contrast agents in NMR imaging. J Comp Tomogr 1981; 5: 543-547.
29. O'Connor JPB, Naish JH, Jackson A, et al. Comparison of Normal Tissue R-1 and R-2* Modulation by Oxygen and Carbogen. Magn Reson Med 2009; 61: 75-83.
30. Matsumoto K, Bernardo M, Subramanian S, Choyke P, Mitchell JB, Krishna MC, Lizak MJ,. MR assessment of changes of tumor in response to hyperbaric oxygen treatment. Magn Reson Med 2006; 56: 240-246.
31. Zhao D, Jiang L, Mason RP,. Measuring changes in tumor oxygenation. Methods Enzymol 2004; 386: 378-418.
32. 19F MRI in a rat model. Magn Reson Med 2011; 66: 1722-1730.
33. 19F MRI oximetry. Magn Reson Mat Phys Biol Med 2010; 23: 217-226.
34. Magat J, Jordan BF, Cron GO, Gallez B,. Noninvasive mapping of spontaneous fluctuations in tumor oxygenation using F-19 MRI. Med Phys 2010; 37: 5434-5441.
35. Peschke P, Hahn EW, Wenz F, Lohr F, Braunschweig F, Wolber G, Zuna I, Wannenmacher M,. Differential sensitivity of three sublines of the rat dunning prostate tumor system R3327 to radiation and/or local tumor hyperthermia. Radiat Res 1998; 150: 423-430.
36. Peschke P, Karger CP, Scholz M, Debus J, Huber PE,. Relative biological effectiveness of carbon ions for local tumor control of a radioresistant prostate carcinoma in the rat. Int J Radiat Oncol Biol Phys 2011; 79: 239-246.
37. Pidikiti R, Stojadinovic S, Speiser M, Song KH, Hager F, Saha D, Solberg TD,. Dosimetric characterization of an image-guided stereotactic small animal irradiator. Phys Med Biol 2011; 56: 2585-2599.
38. Zhao D, Ran S, Constantinescu A, Hahn EW, Mason RP,. Tumor oxygen dynamics: correlation of in vivo MRI with histological findings. Neoplasia 2003; 5: 308-318.
39. Bourke VA, Zhao D, Gilio J, Chang C-H, Jiang L, Hahn EW, Mason RP,. Correlation of radiation response with tumor oxygenation in the dunning prostate R3327-AT1 tumor. Int J Radiat Oncol Biol Phys 2007; 67: 1179-1186.
40. Procissi D, Claus F, Burgman P, Koziorowski J, Chapman JD, Thakur SB, Matei C, Ling CC, Koutcher JA,. In vivo F-19 magnetic resonance spectroscopy and chemical shift imaging of tri-fluoro-nitroimidazole as a potential hypoxia reporter in solid tumors. Clin Cancer Res 2007; 13: 3738-3747.
41. 19F PBSR EPI of hexafluorobenzene. Magn Reson Imaging 1997; 15: 971-981.
42. Hunjan S, Zhao D, Constantinescu A, Hahn EW, Antich PP, Mason RP,. Tumor Oximetry: demonstration of an enhanced dynamic mapping procedure using fluorine-19 echo planar magnetic resonance imaging in the Dunning prostate R3327-AT1 rat tumor. Int J Radiat Oncol Biol Phys 2001; 49: 1097-1108.
43. Nozue M, Lee I, Yuan F, et al. Interlaboratory variation in oxygen tension measurement by Eppendorf "Histograph" and comparison with hypoxic marker. J Surg Oncol 1997; 66: 30-38.
44. Fan X, River JN, Zamora M, Al-Hallaq HA, Karczmar GS,. Effect of carbogen on tumor oxygenation: combined fluorine-19 and proton MRI measurements. Int J Radiat Oncol Biol Phys 2002; 54: 1202-1209.
45. 2) inside tumors? Magn Reson Med 2002; 48: 980-986.
46. Hoskin PJ, Carnell DM, Taylor NJ, et al. Hypoxia in prostate cancer: correlation of BOLD-MRI with pimonidazole immunohistochemistry-initial observations. Int J Radiat Oncol Biol Phys 2007; 68: 1065-1071.
47. 2* enough to assess oxygenation? Quantitative blood oxygen level dependent analysis in brain tumor. Radiology 2012; 262: 495-502.
48. Robinson SP, Rijken PF, Howe FA, McSheehy PM, van der Sanden BP, Heerschap A, Stubbs M, Van Der Kogel AJ, Griffiths JR,. Tumor vascular architecture and function evaluated by non-invasive susceptibility MRI methods and immunohistochemistry. J Magn Reson Imaging 2003; 17: 445-454.
49. Winter JD, Akens MK, Cheng H-LM,. Quantitative MRI assessment of VX2 tumour oxygenation changes in response to hyperoxia and hypercapnia. Phys Med Biol 2011; 56: 1225.
50. Ding Y, Mason RP, McColl RW, Yuan Q, Hallac RR, Sims RD, Weatherall PT,. Simultaneous measurement of TOLD and BOLD effects in abdominal tissue oxygenation level studies. J Magn Reson Imaging 2013; 38: 1230-1236.
51. Remmele S, Sprinkart AM, Müller A, et al. Dynamic and simultaneous MR measurement of R(1) and R(2) * changes during respiratory challenges for the assessment of blood and tissue oxygenation. Magn Reson Med 2013; 70: 136-146.
52. Arias N, Pacheco-Torres J, Lõpez-Larrubia P,. Predicting response to hyperbaric oxygen radiotherapy treatment in high grade gliomas using Magnetic Resonance Imaging techniques. In Proceedings of the 20th Annual Meeting of ISMRM, Melbourne, Australia, 2012. p. 852.
53. Mason RP, Antich PP, Babcock EE, Constantinescu A, Peschke P, Hahn EW,. Non-invasive determination of tumor oxygen tension and local variation with growth. Int J Radiat Oncol Biol Phys 1994; 29: 95-103.
54. Gu Y, Bourke V, Kim JG, Constantinescu A, Mason RP, Liu H,. Dynamic response of breast tumor oxygenation to hyperoxic respiratory challenge monitored with three oxygen-sensitive parameters. Appl Opt 2003; 42: 1-8.
55. Zhao D, Constantinescu A, Hahn EW, Mason RP,. Tumor oxygen dynamics with respect to growth and respiratory challenge: investigation of the Dunning prostate R3327-HI tumor. Radiat Res 2001; 156: 510-520.
56. Timmerman R, Paulus R, Galvin J, et al. Stereotactic body radiation therapy for inoperable early stage lung cancer. JAMA 2010; 303: 1070-1076.
57. Carlson DJ, Keall PJ, Loo BW, Chen ZJ, Brown JM,. Hypofractionation results in reduced tumor cell kill compared to conventional fractionation for tumors with regions of hypoxia. Int J Radiat Oncol Biol Phys 2011; 79: 1188-1195.
58. Brown JM, Diehn M, Loo BW Jr,. Stereotactic Ablative Radiotherapy Should Be Combined With a Hypoxic Cell Radiosensitizer. Int J Radiat Oncol Biol Phys 2010; 78: 323-327.
59. Yuan Q, Ding Y, Hallac RR, Sims RD, Weatherall PT, Boike T, Timmerman R, Mason RP,. Feasibility of BOLD magnetic resonance imaging of lung tumors at 3 T. In Proceedings of the 18th Annual Meeting of ISMRM, Stockholm, Sweden, 2010. p. 1093.
60. Zhang Z, Hallac RR, Peschke P, Mason RP,. A noninvasive tumor oxygenation imaging strategy using magnetic resonance imaging of endogenous blood and tissue water. Magn Reson Med 2014; 71: 561-569.